Epidemiology of Taenia Saginata Taeniosis

Epidemiology of Taenia Saginata Taeniosis

Dermauw et al. Parasites & Vectors (2018) 11:578 https://doi.org/10.1186/s13071-018-3163-3 REVIEW Open Access Epidemiology of Taenia saginata taeniosis/ cysticercosis: a systematic review of the distribution in southern and eastern Africa Veronique Dermauw1* , Pierre Dorny1,2, Uffe Christian Braae3, Brecht Devleesschauwer4,5, Lucy J. Robertson6, Anastasios Saratsis7 and Lian F. Thomas8,9 Abstract Background: The beef tapeworm, Taenia saginata, causing cysticercosis in bovines and taeniosis in humans, is thought to have a global distribution. In eastern and southern Africa, cattle production plays a crucial role in the economy, but a clear overview of the prevalence of T. saginata in the region is still lacking. This review aims to summarize existing knowledge on T. saginata taeniosis and bovine cysticercosis distribution in eastern and southern Africa. Methods: A systematic review was conducted, that gathered published and grey literature, including OIE reports, concerning T. saginata taeniosis and bovine cysticercosis in eastern and southern Africa published between January 1st, 1990 and December 31st, 2017. Results: A total of 1232 records were initially retrieved, with 78 full text articles retained for inclusion in the database. Unspecified taeniosis cases were reported for Angola, Ethiopia, Kenya, Madagascar, Malawi, South Africa, Tanzania, Uganda and Zambia, whereas T. saginata taeniosis cases were found for Ethiopia, Kenya, South Africa, Tanzania, Zambia and Zimbabwe. The prevalence of taeniosis ranged between 0.2–8.1% based on microscopy, and between 0.12–19.7% based on coproAg-ELISA. In Ethiopia, the percentage of tapeworm self-reporting was high (45.0–64.2%), and a substantial number of anthelmintic treatments were reported to be sold in towns. The presence of bovine cysticercosis was reported in all 27 countries/territories included in the study, except for Rwanda and Somalia, Comoros, Madagascar, Mauritius, Mayotte, Seychelles and Socotra. The prevalence of cysticercosis ranged between 0.02–26.3% based on meat inspection, and between 6.1–34.9% based on Ag-ELISA. Conclusions: Although T. saginata has been reported in the majority of countries/territories of the study area, T. saginata taeniosis/cysticercosis remains a largely ignored condition, probably due to the absence of symptoms in cattle, the lack of data on its economic impact, and the fact that human taeniosis is considered a minor health problem. However, the occurrence of bovine cysticercosis is a clear sign of inadequate sanitation, insufficient meat inspection, and culinary habits that may favour transmission. Measures to reduce transmission of T. saginata are therefore warranted and the infection should be properly monitored. Keywords: Taenia saginata, Cestode, Beef tapeworm, Taeniosis, Bovine cysticercosis, Eastern Africa, Southern Africa * Correspondence: [email protected] 1Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Dermauw et al. Parasites & Vectors (2018) 11:578 Page 2 of 12 Background the parasite is thought to be of particular relevance here. The beef tapeworm, Taenia saginata, utilizes bovines as In the area, bovines are essential for the livelihoods of intermediate hosts and humans as final hosts. Although smallholders, serving as a source of food, draft power tapeworm infections have been reported since ancient and manure, as well as acting as a financial buffer for times [1], it was not until 1782 [2] that differentiation of challenging times. Although there are indications of the T. saginata from the other well-known meat-transmitted widespread presence of the parasite in at least some human tapeworm, Taenia solium, was established. countries in this region (e.g. Ethiopia: [15–17]), an Furthermore, it was not until 1871 that the role of cattle extensive overview of its distribution in this region, as intermediate hosts for the parasite was established, along with epidemiological considerations regarding its with “measly” beef being reported as the source of infec- presence, is still lacking. Our aim was therefore to gather tion in patients [3]. recent information on the presence of T. saginata in Ingestion of raw or undercooked infected beef is indeed eastern and southern Africa. the mode of transmission of this zoonotic parasite to humans, in whom it develops to its adult form, a several Methods metres long segmented worm consisting of a scolex with Search strategy four suckers, neck and strobila, i.e. a chain of proglottids A systematic review of published literature was conducted [4]. In contrast to T. solium, the gravid proglottids of T. to collect data on the occurrence, prevalence, and geo- saginata, which contain thousands of embryonated eggs, graphical distribution of bovine cysticercosis and human are mobile and can migrate from the anus independently taeniosis in eastern and southern Africa, published between of, as well as during, defaecation [5]. Eggs are then shed January 1st, 1990 and December 31st, 2017. For the pur- into the environment, and cattle become infected through pose of this study, eastern and southern Africa was defined grazing contaminated pastures, or ingesting contaminated as the area covered by the following countries/territories: fodder or water. After hatching, and penetration of the Angola, Botswana, Burundi, Comoros, Djibouti, Eritrea, intestinal wall, the oncospheres reach the general circula- Ethiopia, Kenya, Lesotho, Madagascar, Malawi, Mauritius, tion, distributing them throughout the body where they Mayotte (French), Mozambique, Namibia, Réunion develop into cysticerci [4]. Common predilection sites for (French), Rwanda, Seychelles, Socotra (Yemini), Somalia T. saginata cysticerci include the heart and masseter (including the autonomous regions Puntland and muscles [6]. Somaliland), South Africa, Swaziland, Tanzania (including In both intermediate and definitive hosts, T. saginata the semi-autonomous region of Zanzibar), Uganda, Zambia causes few symptoms. In humans, infection is usually and Zimbabwe. The PRISMA guidelines were followed characterized by anal pruritus due the active migration whilst conducting the review [18] (Additional file 1). The of T. saginata proglottids and some mild abdominal pain search protocol can be found in Additional file 2. [7]. Nevertheless, the (potential) presence of a tapeworm The international bibliographic databases PubMed in the body can cause distress [8], and some people even (http://www.ncbi.nlm.nih.gov/pubmed) and Web of Sci- suffer from a pathological fear of tapeworms, often en- ence (http://ipscience.thomsonreuters.com/product/web- couraged by horror stories circulating in popular media of-science/) were searched using the following search or books [9, 10]. Moreover, although rare, complications phrase: (cysticerc* OR cisticerc* OR “C. bovis” OR tae- due to taeniosis, such as appendicitis, have been re- nia* OR tenia* OR saginata OR taeniosis OR teniosis OR ported [11]. In cattle, the infection is generally asymp- taeniasis OR ténia OR taeniid OR cysticerque) AND tomatic but nevertheless may incur great economic (Angola OR Botswana OR Burundi OR Comoros OR losses for the meat sector due to carcass condemnation Djibouti OR Eritrea OR Ethiopia OR Kenya OR Lesotho or treatment upon detection of cysticerci during meat OR Madagascar OR Malawi OR Mauritius OR Mayotte inspection, as well as related insurance costs [12, 13]. OR Mozambique OR Namibia OR Réunion OR Rwanda Taenia saginata is distributed globally, with the OR Seychelles OR Socotra OR Somalia OR South Africa parasite occurring in both developed and developing OR Swaziland OR Tanzania OR Uganda OR Zanzibar countries, although less frequently in countries where OR Zambia OR Zimbabwe OR “East Africa” OR “Horn cultural preferences limit consumption of bovids or of Africa” OR “Southern Africa” OR Puntland OR where adequate sanitary infrastructure reduces the likeli- Somaliland). hood of bovids ingesting human faecal matter. Thus, the Furthermore, a range of databases for grey literature prevalence of human taeniosis and bovine cysticercosis and MSc/PhD thesis documents were searched using are considered particularly high in Africa, Latin America keywords from the above search phrase (the full list and some parts of Asia [4]. of databases is presented in Additional file 3). Data In eastern and southern Africa, the cattle population on bovine cysticercosis from the different scientific was estimated at a massive 20.6 million in 2016 [14], so databases were complemented with data from OIE Dermauw et al. Parasites & Vectors (2018) 11:578 Page 3 of 12 databases “Handistatius” (1996–2004) and “WAHIS” on title and, thereafter, abstract. During title screen- (2005) [19, 20]. Finally, reference lists of reviews on ing, 987 records were excluded, and a further 85 the topic were screened and additional relevant

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